A-to-I mRNA editing in fungi: occurrence, function, and evolution
- 432 Downloads
A-to-I RNA editing is an important post-transcriptional modification that converts adenosine (A) to inosine (I) in RNA molecules via hydrolytic deamination. Although editing of mRNAs catalyzed by adenosine deaminases acting on RNA (ADARs) is an evolutionarily conserved mechanism in metazoans, organisms outside the animal kingdom lacking ADAR orthologs were thought to lack A-to-I mRNA editing. However, recent discoveries of genome-wide A-to-I mRNA editing during the sexual stage of the wheat scab fungus Fusarium graminearum, model filamentous fungus Neurospora crassa, Sordaria macrospora, and an early diverging filamentous ascomycete Pyronema confluens indicated that A-to-I mRNA editing is likely an evolutionarily conserved feature in filamentous ascomycetes. More importantly, A-to-I mRNA editing has been demonstrated to play crucial roles in different sexual developmental processes and display distinct tissue- or development-specific regulation. Contrary to that in animals, the majority of fungal RNA editing events are non-synonymous editing, which were shown to be generally advantageous and favored by positive selection. Many non-synonymous editing sites are conserved among different fungi and have potential functional and evolutionary importance. Here, we review the recent findings about the occurrence, regulation, function, and evolution of A-to-I mRNA editing in fungi.
KeywordsRNA modification Deamination Adenosine Inosine Sexual reproduction Fusarium graminearum Neurospora crassa Epigenetic Adaptation ADAR ADAT Non-synonymous editing
We thank Ruonan Hei for assistance in preparing the illustrations and Drs. Cong Jiang, Qinhu Wang, and Chenfang Wang for fruitful discussions. We also thank Dr. Larry Dunkle at Purdue University for language editing the manuscript. This work was supported by grants from the National Science Fund for Excellent Young Scholars (Grant 31622045) and the National Youth Talent Support Program (Z111021802) to HL, and grants from the US Wheat Barley Scab Initiative and National Science Foundation to JX.
Compliance with ethical standards
Conflict of interest
The authors declare no competing financial interests.
- 11.Holley RW, Everett GA, Madison JT, Zamir A (1965) Nucleotide sequences in the yeast alanine transfer ribonucleic acid. J Biol Chem 240:2122–2128Google Scholar
- 25.Wang Q, Jiang C, Liu H, Xu J-R (2016) ADAR-independent A-to-I RNA editing is generally adaptive for sexual reproduction in fungi. bioRxiv: 059725Google Scholar
- 32.Pöggeler S, Nowrousian M, Teichert I, Beier A, Kück U (2018) Fruiting-body development in ascomycetes. In: Physiology and genetics, 2nd edn. Springer, Berlin, pp 1–56Google Scholar
- 35.Liscovitch-Brauer N et al (2017) Trade-off between transcriptome plasticity and genome evolution in cephalopods. Cell 169(191–202):e11Google Scholar
- 64.Kroger B, Vinther J, Fuchs D (2011) Cephalopod origin and evolution: a congruent picture emerging from fossils, development and molecules: extant cephalopods are younger than previously realised and were under major selection to become agile, shell-less predators. BioEssays 33:602–613CrossRefGoogle Scholar
- 66.Smith KM, Phatale PA, Bredeweg EL, Connolly LR, Pomraning KR, Freitag M (2012) Epigenetics of filamentous fungi Epigenetic regulation and epigenomics. Wiley, Hoboken, pp 1063–1107 (Curr Top Encycl Mol Cell Biol) Google Scholar
- 70.Pomraning KR, Connolly LR, Whalen JP, Smith KM, Freitag M (2013) Repeat-induced point mutation, DNA methylation and heterochromatin in Gibberella zeae (anamorph: Fusarium graminearum). In: Fusarium: genomics, molecular and cellular biology, 2nd edn. Horizon Scientific Press, Poole, p 93Google Scholar
- 71.Schmitt I (2011) 8 Fruiting body evolution in the ascomycota: a molecular perspective integrating lichenized and non-lichenized groups. In: Evolution of fungi and fungal-like organisms, 2nd edn. Springer, Berlin, pp 187–204Google Scholar
- 74.Wu B et al (2018) Substrate-specific differential gene expression and RNA editing in the Brown Rot Fungus Fomitopsis pinicola. Appl Environ Microbiol 84(16). pii: e00991–18. https://doi.org/10.1128/AEM.00991-18
- 82.Burt A (2000) Perspective: sex, recombination, and the efficacy of selection—was Weismann right? Evolution 54:337–351Google Scholar